Skip to main content
Log in

Molecular prevalence and associated risk factors of Theileria annulata infections in dromedary camels in Egypt

  • Regular Articles
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

Theileria annulata (T. annulata) is an intracellular protozoan, transmitted by ixodid ticks of the genus Hyalomma and affects camels. There are few epidemiological data on T. annulata infection and its associated risk factors in Egyptian camels. Thus, the present study aimed to determine the prevalence of T. annulata in camels using PCR and assess the associated risk factors for infection. A total of 380 blood samples were collected from camels raising in three Egyptian governorates and examined by PCR assay targeting 30-kDa gene to detect the presence of T. annulata infection, beside statistical analysis of associated factors. The results revealed presence of T. annulata with overall prevalence of 21.1%. In addition, the univariate analysis revealed significant (P<0.05) association between prevalence of T. annulata in camels and locality, age, sex, tick infestation, and application of acaricides. Whereas the prevalence of T. annulata was higher in camels of age group >6 to 10 years (38%), females (25.7%) and in infested camels with ticks (29%) and in case of absence of acaricides application (25%). In contrast, the body condition of camels had not significant effect on prevalence of theileriosis in camels. The current study concluded that T. annulata is prevalent in Egyptian camels and that a tick control program is required to reduce the risk of infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article.

References

  • Abdelwahab, G.E., Tigani-Asil, E., Yusof, M.F., Abdullah, Z.S., Rifat, J.F., Al Hosani, M.A., Almuhairi, S.S., and Khalafalla, A.I., 2019. Salmonella enterica and Theileria co-infection in dromedary camels (Camelus dromedarius) in UAE, Open Veterinary Journal, 9, 263–268

    Article  PubMed  PubMed Central  Google Scholar 

  • Alsaadi, H.H., and Faraj, A.A., 2020a. Molecular study and effect of risk factors on infection rates of Theileriosis in camels in middle of Iraq, Plant Archives, 20, 1349-1354

    Google Scholar 

  • Alsaadi, H.H., and Faraj, A.A., 2020b. Traditional Study and seroprevalence of Theileria spp. in camels in Middle of Iraq (Wasit, Al-Qadisiyah and Al-Najaf AlAshraf) Plant Archives, 20, 4158-4141

    Google Scholar 

  • Alsubki, R.A., Albohairy, F.M., Attia, K.A., Kimiko, I., Selim, A., and Sayed-Ahmed, M.Z., 2022. Assessment of seroprevalence and associated risk factors for anaplasmosis in Camelus dromedarius, Veterinary Sciences, 9, 57

    Article  PubMed  PubMed Central  Google Scholar 

  • Aslam, F., Saleem, G., Ashraf, K., Hafeez, M.A., and Saqib, M., 2023. Identification and molecular characterization of theileria annulata with associated risk factors in naturally infected camels from selected districts in Punjab, Pakistan, Pakistan Veterinary Journal, 43, 4.

    Google Scholar 

  • Chauhan, H., Patel, B., Bhagat, A., Patel, M., Patel, S., Raval, S., Panchasara, H., Shrimali, M., Patel, A., and Chandel, B., 2015. Comparison of molecular and microscopic technique for detection of Theileria annulata from the field cases of cattle, Veterinary world, 8, 1370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • d'Oliveira, C., Van Der Weide, M., Habela, M.A., Jacquiet, P., and Jongejan, F., 1995. Detection of Theileria annulata in blood samples of carrier cattle by PCR, Journal of Clinical Microbiology, 33, 2665-2669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Defaye, B., Moutailler, S., Pasqualini, V., and Quilichini, Y., 2022. Distribution of tick-borne pathogens in domestic animals and their ticks in the countries of the Mediterranean basin between 2000 and 2021: A systematic review, Microorganisms, 10, 1236

    Article  PubMed  PubMed Central  Google Scholar 

  • El-Naga, T.R.A., and Barghash, S., 2016. Blood parasites in camels (Camelus dromedarius) in Northern West Coast of Egypt, J. Bacteriol. Parasitol, 7, 258

    Google Scholar 

  • Elhaig, M.M., Youssef, A.I., and El-Gayar, A.K., 2013. Molecular and parasitological detection of Trypanosoma evansi in camels in Ismailia, Egypt, Veterinary Parasitology, 198, 214-218

    Article  CAS  PubMed  Google Scholar 

  • Gebrekidan, H., Hailu, A., Kassahun, A., Rohoušová, I., Maia, C., Talmi-Frank, D., Warburg, A., and Baneth, G., 2014. Theileria infection in domestic ruminants in northern Ethiopia, Veterinary Parasitology, 200, 31-38

    Article  CAS  PubMed  Google Scholar 

  • Hamed, M.I., Zaitoun, A.M., El-Allawy, T.A., and Mourad, M.I., 2011. Investigation of Theileria camelensis in camels infested by Hyalomma dromedarii ticks in Upper Egypt, Journal of Advanced Veterinary Research, 1, 4-7

    Google Scholar 

  • Hosmer, D.W., Lemeshow, S., and Sturdivant, R.X., 2000. Introduction to the logistic regression model, Applied logistic regression, 2, 1-30

    Google Scholar 

  • Ismael, A.B., Swelum, A.A., Khalaf, A.F., and Abouheif, M.A., 2014. Clinical, haematological and biochemical alterations associated with an outbreak of theileriosis in dromedaries (Camelus dromedarius) in Saudi Arabia, Pak. Vet. J, 34, 209-213

    Google Scholar 

  • Karimi, A., Rahbari, S., and Yousefi, A., 2015. Blood parasites of camels from central regions of Iran: comparative evaluation of various detection techniques and serum protein components, Journal of Advances in Parasitology, 2, 1-4

    Article  Google Scholar 

  • Kaufmann, B.A., 2005. Reproductive performance of camels (Camelus dromedarius) under pastoral management and its influence on herd development, Livestock Production Science, 92, 17-29

    Article  Google Scholar 

  • Mirahmadi, H., Ghaderi, A., Barani, S., Alijani, E., Mehravaran, A., and Shafiei, R., 2022. Prevalence of camel babesiosis in southeast of Iran, Veterinary Medicine and Science, 8, 343-348

    Article  PubMed  Google Scholar 

  • Mohsin, M., Hameed, K., Kamal, M., Ali, A., Rafiq, N., Usman, T., Khan, W., Abbasi, A.A., Khan, R.U., and Yousafzai, G.J., 2022. Prevalence and risk factors assessment of theileriosis in livestock of Malakand Division, Pakistan, Journal of the Saudi Society of Agricultural Sciences, 21, 242-247

    Article  Google Scholar 

  • Nijhof, A.M., Bodaan, C., Postigo, M., Nieuwenhuijs, H., Opsteegh, M., Franssen, L., Jebbink, F., and Jongejan, F., 2007. Ticks and associated pathogens collected from domestic animals in the Netherlands, Vector-borne and zoonotic diseases, 7, 585-596

    Article  PubMed  Google Scholar 

  • Patel, G., Shanker, D., Jaiswal, A.K., Sudan, V., and Verma, S.K., 2013. Prevalence and seasonal variation in ixodid ticks on cattle of Mathura district, Uttar Pradesh, Journal of Parasitic Diseases, 37, 173-176

    Article  PubMed  Google Scholar 

  • Pourhoseingholi, M.A., Vahedi, M., and Rahimzadeh, M., 2013. Sample size calculation in medical studies, Gastroenterology and Hepatology from bed to bench, 6, Hepatol Bed Bench 2016 (2011): 2014-2017

    Google Scholar 

  • Rutter, T., 1967. Diseases of camels. 2. Protozoan diseases, Vet. Bull, 37, 611-618

    Google Scholar 

  • Salih, D., Hassan, S., and El Hussein, A., 2007. Comparisons among two serological tests and microscopic examination for the detection of Theileria annulata in cattle in northern Sudan, Preventive veterinary medicine, 81, 323-326

    Article  CAS  PubMed  Google Scholar 

  • Sazmand, A., and Joachim, A., 2017. Parasitic diseases of camels in Iran (1931–2017)–a literature review, Parasite, 24, 21.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schnittger, L., Ganzinelli, S., Bhoora, R., Omondi, D., Nijhof, A.M., and Florin-Christensen, M., 2022. The Piroplasmida Babesia,Cytauxzoon, and Theileria in farm and companion animals: Species compilation, molecular phylogeny, and evolutionary insights Parasitology Research, 121, 1207-1245

    Article  PubMed  Google Scholar 

  • Selim, A., and Abdelhady, A., 2020a. The first detection of anti-West Nile virus antibody in domestic ruminants in Egypt, Tropical Animal Health and Production, 52, 3147-3151

    Article  PubMed  Google Scholar 

  • Selim, A., and Abdelhady, A., 2020b. Neosporosis among Egyptian camels and its associated risk factors, Tropical Animal Health and Production, 52, 3381-3385

    Article  PubMed  Google Scholar 

  • Selim, A., Alafari, H.A., Attia, K., AlKahtani, M.D., Albohairy, F.M., and Elsohaby, I., 2022a. Prevalence and animal level risk factors associated with Trypanosoma evansi infection in dromedary camels, Scientific Reports, 12, 8933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selim, A., and Ali, A.-F., 2020. Seroprevalence and risk factors for C. burentii infection in camels in Egypt, Comparative Immunology, Microbiology and Infectious Diseases, 68, 101402

    Article  PubMed  Google Scholar 

  • Selim, A., Ali, A.-F., and Ramadan, E., 2019. Prevalence and molecular epidemiology of Johne’s disease in Egyptian cattle, Acta tropica, 195, 1-5

    Article  CAS  PubMed  Google Scholar 

  • Selim, A., Alsubki, R.A., Albohairy, F.M., Attia, K.A., and Kimiko, I., 2022b. A survey of bluetongue infection in one-humped camels (Camelus Dromedarius); seroprevalence and risk factors analysis, BMC Veterinary Research, 18, 1-6

    Article  Google Scholar 

  • Selim, A., Attia, K.A., Alsubki, R.A., Kimiko, I., and Sayed-Ahmed, M.Z., 2022c. Cross-sectional survey on Mycobacterium avium Subsp. paratuberculosis in Dromedary Camels: Seroprevalence and risk factors, Acta Tropica, 226, 106261

  • Selim, A., El-Haig, M., Galila, E.S., and Gaede, W., 2013. Direct detection of Mycobacterium avium subsp. Paratuberculosis in bovine milk by multiplex Real-time PCR, Animal Science Papers and Reports, 31, 291-302

    CAS  Google Scholar 

  • Selim, A., and Khater, H., 2020. Seroprevalence and risk factors associated with Equine piroplasmosis in North Egypt, Comparative immunology, microbiology and infectious diseases, 73, 101549

    Article  PubMed  Google Scholar 

  • Selim, A., Khater, H., and Almohammed, H.I., 2021a. A recent update about seroprevalence of ovine neosporosis in Northern Egypt and its associated risk factors, Scientific Reports, 11, 14043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selim, A., Manaa, E., and Khater, H., 2021b. Molecular characterization and phylogenetic analysis of lumpy skin disease in Egypt, Comparative immunology, microbiology and infectious diseases, 79, 101699

    Article  CAS  PubMed  Google Scholar 

  • Selim, A., Manaa, E.A., Waheed, R.M., and Alanazi, A.D., 2021c. Seroprevalence, associated risk factors analysis and first molecular characterization of chlamydia abortus among Egyptian sheep, Comparative immunology, microbiology and infectious diseases, 74, 101600

    Article  CAS  PubMed  Google Scholar 

  • Selim, A., Marawan, M.A., Abdelhady, A., and Wakid, M.H., 2023. Seroprevalence and Potential Risk Factors of Toxoplasma gondii in Dromedary Camels, Agriculture, 13, 129

    Article  Google Scholar 

  • Selim, A., Marawan, M.A., Ali, A.-F., Manaa, E., and AbouelGhaut, H.A., 2020. Seroprevalence of bovine leukemia virus in cattle, buffalo, and camel in Egypt, Tropical Animal Health and Production, 52, 1207-1210

    Article  PubMed  Google Scholar 

  • Selim, A., Weir, W., and Khater, H., 2022d. Prevalence and risk factors associated with tropical theileriosis in Egyptian dairy cattle, Veterinary world, 15, 919

    Article  PubMed  PubMed Central  Google Scholar 

  • Selim, A.M., Elhaig, M.M., Moawed, S.A., and El-Nahas, E., 2018. Modeling the potential risk factors of bovine viral diarrhea prevalence in Egypt using univariable and multivariable logistic regression analyses, Veterinary world, 11, 259

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh, N.K., and Rath, S.S., 2013. Epidemiology of ixodid ticks in cattle population of various agro-climatic zones of Punjab, India, Asian Pacific journal of tropical medicine, 6, 947-951

    Article  PubMed  Google Scholar 

  • Sobhy, H.M., Barghash, S.M., Behour, T.S., and Razin, E.A., 2017. Seasonal fluctuation of trypanosomiasis in camels in North-West Egypt and effect of age, sex, location, health status and vector abundance on the prevalence, Beni-Suef University Journal of Basic and Applied Sciences, 6, 64-68

    Article  Google Scholar 

  • Swelum, A.A., Ismael, A.B., Khalaf, A.F., and Abouheif, M.A., 2014. Clinical and laboratory findings associated with naturally occurring babesiosis in dromedary camels, Bulletin of the Veterinary Institute in Pulawy, 58, 229-233

    Article  CAS  Google Scholar 

  • Tamimi, N.S.M., 2022. Effects of Theileria Annulata Infection on Hematology, Lipid Profile, and Milk Properties of Iraqi Dromedary Camels, Annals of the Romanian Society for Cell Biology, 26, 1804-1816

    Google Scholar 

  • Theodory, T.F., and Malipula, M., 2014. Climate change and socio-economic vulnerability among Maasai pastoral communities in Northern Tanzania, Journal of Policy and Leadership, 2, 20-22

    Google Scholar 

  • Tibary, A., Abdelhaq, A., and Abdelmalek, S., 2005. Factors affecting reproductive performance of camels at the herd and individual level, Desertification combat and food safety: the added value of camel producers, Ashkabad, Turkmenistan, 19-21 April 2004, 97-114

  • Ullah, K., Numan, M., Alouffi, A., Almutairi, M.M., Zahid, H., Khan, M., Islam, Z.U., Kamil, A., Safi, S.Z., and Ahmed, H., 2022. Molecular Characterization and assessment of risk factors associated with Theileria annulata infection, Microorganisms, 10, 1614

    Article  PubMed  PubMed Central  Google Scholar 

  • Ullah, R., Shams, S., Khan, M.A., Ayaz, S., Akbar, N.u., Din, Q.u., Khan, A., Leon, R., and Zeb, J., 2021. Epidemiology and molecular characterization of Theileria annulata in cattle from central Khyber Pakhtunkhwa Pakistan, PloS one, 16, e0249417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youssef, S.Y., Yasien, S., Mousa, W.M.A., Nasr, S.M., El-Kelesh, E.A.M., Mahran, K.M., and Abd-El-Rahman, A.H., 2015. Vector identification and clinical, hematological, biochemical, and parasitological characteristics of camel (Camelus dromedarius) theileriosis in Egypt, Tropical Animal Health and Production, 47, 649-656

    Article  PubMed  Google Scholar 

  • Zeb, J., Shams, S., Din, I.U., Ayaz, S., Khan, A., Nasreen, N., Khan, H., Khan, M.A., and Senbill, H., 2020. Molecular epidemiology and associated risk factors of Anaplasma marginale and Theileria annulata in cattle from North-western Pakistan, Veterinary Parasitology, 279, 109044

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia for the financial support of this research (Grant No: 4275).

Funding

This work was supported through the Annual Funding track by the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia (Grant No: 4275).

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization, methodology, formal analysis, investigation, resources, data curation, writing-original draft preparation, A.S., O.A.A., H.S.G., M.M., M.S. and A.A.; writing-review and editing, A.S., M.M., O.A.A., H.S.G., M.S. and A.A.; project administration, M.M.; funding acquisition, A.S., M.M., O.A.A., H.S.G., M.S. and A.A. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Abdelfattah Selim or Mohamed Marzok.

Ethics declarations

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Conflict of interest

The authors declare that they have no competing of interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Selim, A., Alshammari, A., Marzok, M. et al. Molecular prevalence and associated risk factors of Theileria annulata infections in dromedary camels in Egypt. Trop Anim Health Prod 55, 335 (2023). https://doi.org/10.1007/s11250-023-03767-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11250-023-03767-1

Keywords

Navigation